Origins of the 2009 H1N1 influenza pandemic in swine in Mexico

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Mena, Ignacio ^a   Nelson, Martha I ^b   Quezada Monroy, Francisco ^c   Dutta, Jayeeta ^a   Cortes Fernández, Refugio ^c   Lara Puente, J Horacio ^c   Castro Peralta, Felipa ^c   Cunha, Luis F ^a   Trovão, Nídia S ^a,b,d   Lozano Dubernard, Bernardo ^c   Rambaut, Andrew ^b,e   Van Bakel, Harm ^a   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c Laboratorio Avi Mex   (Mexico)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HUMAN; INFLUENZA A (H1N1); MEXICO; MOLECULAR GENETICS; NONHUMAN; PANDEMIC; PHYLOGENY; PIG; RISK FACTOR; SPATIAL ANALYSIS; VIRUS TRANSMISSION; ANIMAL; CLASSIFICATION; DNA SEQUENCE; GENETICS; INFLUENZA; INFLUENZA A VIRUS (H1N1); ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; ORTHOMYXOVIRUS INFECTION; SWINE DISEASE; VETERINARY; VIROLOGY; ZOONOSIS;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MEXICO; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS; SEQUENCE ANALYSIS, DNA; SWINE; SWINE DISEASES; ZOONOSES;

EID: 84979698202     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.16777     Document Type: Article

References (55)

1. Anderson TK, Nelson MI, Kitikoon P, Swenson SL, Korslund JA, Vincent AL. 2013. Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012. Influenza and Other Respiratory Viruses 7: 42-51. doi: 10.1111/irv.12193
2. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Tatusova T. 2007. FLAN: a web server for influenza virus genome annotation. Nucleic Acids Research 35: W280-284. doi: 10.1093/nar/gkm354
3. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 2008. The influenza virus resource at the National Center for Biotechnology Information. Journal of Virology 82: 596-601. doi: 10.1128/JVI.02005-07
4. Bowman AS, Sreevatsan S, Killian ML, Page SL, Nelson SW, Nolting JM, Cardona C, Slemons RD. 2012. Molecular evidence for interspecies transmission of H3N2pM/H3N2v influenza A viruses at an Ohio agricultural fair, July 2012. Emerging Microbes & Infections 1: e33. doi: 10.1038/emi.2012.33
5. Brockmann D, Helbing D. 2013. The hidden geometry of complex, network-driven contagion phenomena. Science 342: 1337-1342. doi: 10.1126/science.1245200
6. Cappuccio JA, Pena L, Dibárbora M, Rimondi A, Piñeyro P, Insarralde L, Quiroga MA, Machuca M, Craig MI, Olivera V, Chockalingam A, Perfumo CJ, Perez DR, Pereda A. 2011. Outbreak of swine influenza in Argentina reveals a non-contemporary human H3N2 virus highly transmissible among pigs. Journal of General Virology 92: 2871-2878. doi: 10.1099/vir.0.036590-0
7. Chowell G, Echevarría-Zuno S, Viboud C, Simonsen L, Tamerius J, Miller MA, Borja-Aburto VH. 2011. Characterizing the epidemiology of the 2009 influenza A/H1N1 pandemic in Mexico. PLOS Medicine 8: e1000436. doi: 10.1371/journal.pmed.1000436
8. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21. doi: 10.1093/bioinformatics/bts635
9. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969-1973. doi: 10.1093/molbev/mss075
10. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797. doi: 10.1093/nar/gkh340
11. Frank GM, Adalja A, Barbour A, Casadevall A, Dormitzer PR, Duchin J, Hayden FG, Hirsch MS, Hynes NA, Lipsitch M, Pavia AT, Relman DA. 2016. Infectious diseases society of America and gain-of-function experiments with pathogens having pandemic potential. Journal of Infectious Diseases 213: 1359-1361. doi: 10.1093/infdis/jiv474
12. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201. doi: 10.1126/science.1176225
13. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-652. doi: 10.1038/nbt.1883
14. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534-1541. doi: 10.1126/science.1213362
15. Huang X, Madan A. 1999. CAP3: A DNA sequence assembly program. Genome Research 9: 868-877. doi: 10.1101/gr.9.9.868
16. Kawaoka Y, Krauss S, Webster RG. 1989. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. Journal of Virology 63: 4603-4608.
17. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Research 12: 656-664. doi: 10.1101/gr.229202
18. Lakdawala SS, Lamirande EW, Suguitan AL, Wang W, Santos CP, Vogel L, Matsuoka Y, Lindsley WG, Jin H, Subbarao K. 2011. Eurasian-origin gene segments contribute to the transmissibility, aerosol release, and morphology of the 2009 pandemic H1N1 influenza virus. PLOS Pathogens 7: e1002443. doi: 10.1371/journal.ppat.1002443
19. Lam TT, Zhu H, Wang J, Smith DK, Holmes EC, Webster RG, Webby R, Peiris JM, Guan Y. 2011. Reassortment events among swine influenza A viruses in China: implications for the origin of the 2009 influenza pandemic. Journal of Virology 85: 10279-10285. doi: 10.1128/JVI.05262-11
20. Lam TT, Zhou B, Wang J, Chai Y, Shen Y, Chen X, Ma C, Hong W, Chen Y, Zhang Y, Duan L, Chen P, Jiang J, Zhang Y, Li L, Poon LL, Webby RJ, Smith DK, Leung GM, Peiris JS, et al. 2015. Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature 522: 102-105. doi: 10.1038/nature14348
21. Lemey P, Suchard M, Rambaut A. 2009. Reconstructing the initial global spread of a human influenza pandemic: A Bayesian spatial-temporal model for the global spread of H1N1pdm. PLOS Currents 1: RRN1031. doi: 10.1371/currents.RRN1031
22. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, Russell CA, Smith DJ, Pybus OG, Brockmann D, Suchard MA. 2014. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLOS Pathogens 10: e1003932. doi: 10.1371/journal.ppat.1003932
23. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760. doi: 10.1093/bioinformatics/btp324
24. Liang H, Lam TT, Fan X, Chen X, Zeng Y, Zhou J, Duan L, Tse M, Chan CH, Li L, Leung TY, Yip CH, Cheung CL, Zhou B, Smith DK, Poon LL, Peiris M, Guan Y, Zhu H. 2014. Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. Journal of Virology 88: 10864-10874. doi: 10.1128/JVI.01327-14
25. Ma W, Liu Q, Qiao C, del Real G, García-Sastre A, Webby RJ, Richt JA. 2014. North American triple reassortant and Eurasian H1N1 swine influenza viruses do not readily reassort to generate a 2009 pandemic H1N1-like virus. mBio 5: e00919-13. doi: 10.1128/mBio.00919-13
26. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10. doi: 10.14806/ej.17.1.200
27. Minin VN, Suchard MA. 2008a. Counting labeled transitions in continuous-time Markov models of evolution. Journal of Mathematical Biology 56: 391-412. doi: 10.1007/s00285-007-0120-8
28. Minin VN, Suchard MA. 2008b. Fast, accurate and simulation-free stochastic mapping. Philosophical Transactions of the Royal Society B: Biological Sciences 363: 3985-3995. doi: 10.1098/rstb.2008.0176
29. Nelson MI, Lemey P, Vincent A, Lam TT, Detmer S, Viboud C, Suchard MA, Rambaut A, Holmes EC, Gramer M. 2011. Spatial dynamics of human-origin H1 influenza A virus in North American swine. PLOS Path 7: e1002077. doi: 10.1371/journal.ppat.1002077
30. Nelson MI, Wentworth DE, Culhane MR, Vincent AL, Viboud C, LaPointe MP, Lin X, Holmes EC, Detmer SE. 2014. Introductions and evolution of human-origin seasonal influenza a viruses in multinational swine populations. Journal of Virology 88: 10110-10119. doi: 10.1128/JVI.01080-14
31. Nelson MI, Vincent AL. 2015. Reverse zoonosis of influenza to swine: new perspectives on the human-animal interface. Trends in Microbiology 23: 142-153. doi: 10.1016/j.tim.2014.12.002
32. Nelson M, Culhane MR, Rovira A, Torremorell M, Guerrero P, Norambuena J. 2015a. Novel human-like influenza a viruses circulate in swine in Mexico and Chile. PLOS Currents 7. doi: 10.1371/currents.outbreaks.c8b3207c9bad98474eca3013fa933ca6
33. Nelson MI, Schaefer R, Gava D, Cantão ME, Ciacci-Zanella JR, Rejane S. 2015b. Influenza A viruses of human origin in swine, Brazil. Emerg Infect Diseases 21: 1339-1347. doi: 10.3201/eid2108.141891
34. Nelson MI, Viboud C, Vincent AL, Culhane MR, Detmer SE, Wentworth DE, Rambaut A, Suchard MA, Holmes EC, Lemey P. 2015c. Global migration of influenza A viruses in swine. Nature Communications 6: 6696. doi: 10.1038/ncomms7696
35. Nelson MI, Stratton J, Killian ML, Janas-Martindale A, Vincent AL. 2015d. Continual reintroduction of human pandemic H1N1 influenza a viruses into swine in the United States, 2009 to 2014. Journal of Virology 89: 6218-6226. doi: 10.1128/JVI.00459-15
36. Ngo LT, Hiromoto Y, Pham VP, Le HTH, Nguyen HT, Le VT, Takemae N, Saito T. 2012. Isolation of novel triple-reassortant swine H3N2 influenza viruses possessing the hemagglutinin and neuraminidase genes of a seasonal influenza virus in Vietnam in 2010. Influenza and Other Respiratory Viruses 6: 6-10. doi: 10.1111/j.1750-2659.2011.00267.x
37. Pereda A, Rimondi A, Cappuccio J, Sanguinetti R, Angel M, Ye J, Sutton T, Dibárbora M, Olivera V, Craig MI, Quiroga M, Machuca M, Ferrero A, Perfumo C, Perez DR. 2011. Evidence of reassortment of pandemic H1N1 influenza virus in swine in Argentina: are we facing the expansion of potential epicenters of influenza emergence? Influenza and Other Respiratory Viruses 5: 409-412. doi: 10.1111/j.1750-2659.2011.00246.x
38. Perera HK, Wickramasinghe G, Cheung CL, Nishiura H, Smith DK, Poon LL, Perera AK, Ma SK, Sunil-Chandra NP, Guan Y, Peiris JS. 2013. Swine influenza in Sri Lanka. Emerging Infectious Diseases 19: 481-484. doi: 10.3201/eid1903.120945
39. Poonsuk S, Sangthong P, Petcharat N, Lekcharoensuk P. 2013. Genesis and genetic constellations of swine influenza viruses in Thailand. Veterinary Microbiology 167: 314-326. doi: 10.1016/j.vetmic.2013.09.007
40. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, et al. 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science 320: 340-346. doi: 10.1126/science.1154137
41. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125. doi: 10.1038/nature08182
42. Sorrell EM, Wan H, Araya Y, Song H, Perez DR. 2009. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proceedings of the National Academy of Sciences of the United States of America 106: 7565-7570. doi: 10.1073/pnas.0900877106
43. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. doi: 10.1093/bioinformatics/btl446
44. Suchard MA, Rambaut A. 2009. Many-core algorithms for statistical phylogenetics. Bioinformatics 25: 1370-1376. doi: 10.1093/bioinformatics/btp244
45. Takemae N, Parchariyanon S, Damrongwatanapokin S, Uchida Y, Ruttanapumma R, Watanabe C, Yamaguchi S, Saito T. 2008. Genetic diversity of swine influenza viruses isolated from pigs during 2000 to 2005 in Thailand. Influenza and Other Respiratory Viruses 2: 181-189. doi: 10.1111/j.1750-2659.2008.00062.x
46. Taubenberger JK, Morens DM. 2009. Pandemic influenza-including a risk assessment of H5N1. Revue Scientifique Et Technique 28: 187-202. doi: 10.20506/rst.28.1.1879
47. Tinoco YO, Montgomery JM, Kasper MR, Nelson MI, Razuri H, Guezala MC, Azziz-Baumgartner E, Widdowson M-A, Barnes J, Gilman RH, Bausch DG, Gonzalez AE. 2016. Transmission dynamics of pandemic influenza A (H1N1)pdm09 virus in humans and swine in backyard farms in Tumbes, Peru. Influenza and Other Respiratory Viruses 10: 47-56. doi: 10.1111/irv.12329
48. Viboud C, Charu V, Olson D, Ballesteros S, Gog J, Khan F, Grenfell B, Simonsen L. 2014. Demonstrating the use of high-volume electronic medical claims data to monitor local and regional influenza activity in the US. PLOS ONE 9: e102429. doi: 10.1371/journal.pone.0102429
49. Vijaykrishna D, Smith GJ, Pybus OG, Zhu H, Bhatt S, Poon LL, Riley S, Bahl J, Ma SK, Cheung CL, Perera RA, Chen H, Shortridge KF, Webby RJ, Webster RG, Guan Y, Peiris JS. 2011. Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473: 519-522. doi: 10.1038/nature10004
50. Watson SJ, Langat P, Reid SM, Lam TT, Cotten M, Kelly M, Van Reeth K, Qiu Y, Simon G, Bonin E, Foni E, Chiapponi C, Larsen L, Hjulsager C, Markowska-Daniel I, Urbaniak K, Dürrwald R, Schlegel M, Huovilainen A, Davidson I, et al. 2015. Molecular epidemiology and evolution of influenza viruses circulating within European swine between 2009 and 2013. Journal of Virology 89: 9920-9931. doi: 10.1128/JVI.00840-15
51. Weinberg M, Waterman S, Lucas CA, Falcon VC, Morales PK, Lopez LA, Peter C, Gutiérrez AE, Gonzalez ER, Flisser A, Bryan R, Valle EN, Rodriguez A, Hernandez GA, Rosales C, Ortiz JA, Landen M, Vilchis H, Rawlings J, Leal FL, et al. 2003. The U.S.-Mexico Border Infectious Disease Surveillance project: establishing bi-national border surveillance. Emerging Infectious Diseases 9: 97-102. doi: 10.3201/eid0901.020047
52. Yang H, Chen Y, Qiao C, He X, Zhou H, Sun Y, Yin H, Meng S, Liu L, Zhang Q, Kong H, Gu C, Li C, Bu Z, Kawaoka Y, Chen H. 2016. Prevalence, genetics, and transmissibility in ferrets of Eurasian avian-like H1N1 swine influenza viruses. Proceedings of the National Academy of Sciences of the United States of America 113: 392-397. doi: 10.1073/pnas.1522643113
53. Yen HL, Liang CH, Wu CY, Forrest HL, Ferguson A, Choy KT, Jones J, Wong DD, Cheung PP, Hsu CH, Li OT, Yuen KM, Chan RW, Poon LL, Chan MC, Nicholls JM, Krauss S, Wong CH, Guan Y, Webster RG, et al. 2011. Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets. Proceedings of the National Academy of Sciences of the United States of America 108: 14264-14269. doi: 10.1073/pnas.1111000108
54. Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon K, Krauss S, Webster RG. 1999. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. Journal of Virology 73: 8851-8856.
55. Zhu H, Webby R, Lam TT, Smith DK, Peiris JS, Guan Y. 2013. History of Swine influenza viruses in Asia. Current Topics in Microbiology and Immunology 370: 57-68. doi: 10.1007/82_2011_179